Green Synthesis of Silver Nanoparticles as a Wound Healing Agent: a Systematic Review of the Biological Activities
Abstract
Background: The implication of nanotechnology includes silver nanoparticles to medical sciences, and has a revolutionary impact on therapeutic and diagnostics management. Many studies reported that silver nanoparticle (AgNPs) application can accelerate the wound healing process. This study aimed to systematically review the biological activities of silver nanoparticles as a wound-healing agent.
Subjects and Method: This article was a systematic review study conducted by searching for articles from online databases such as EBSCO, PubMed, Science Direct, and World Scientific. Populations: laboratory animals; Intervention: green synthesis of silver nanoparticles; Comparison: a standard ointment for wounds such as povidone-iodine, etc; Outcome: wound healing. The independent variable is the green synthesis of silver nanoparticles, and the dependent variable is wound healing. The inclusion criteria for this study were full articles using an experimental study, with the publication year until 2022. The data extraction was focused on the biological activities of silver nanoparticles and reported following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) recommendations for systematic reviews.
Results: A total of 8 articles reviewed in this study were from countries: Egypt, India, Saudi Arabia, Singapore, and China. The green synthesis of AgNPs was accomplished using a natural aqueous extract from leaves such as Azadirachta indica, Tridax procumbens, the combinations of Catharanthus roseus and Azadirachta indica, Scutellaria barbata, the fungus Fusarium verticillioides, or cyanobacterial platforms (ex: Phormidium sp., Synechocystis sp, and arthrospira sp polysaccharides). All studies were animal-based experimental with wounds infected with bacteria and inflicted in regards to the experiment. All trials resulted in favor of the AgNPs ointment treated group compared to the untreated group or the standard ointment group.
Conclusion: Our review suggested that all studies about the efficacy of AgNPs as wound-healing therapy showed positive results.
Keywords: biological activities, silver nanoparticles, wound healing.
Correspondence: Galih Priambodo. Faculty of Medicine, Universitas Diponegoro. Jl. Prof. Sudarto, Tembalang, Kec. Tembalang, Kota Semarang, Central Java. Email: g2_37@yahoo.co.id. Mobile: 085229998999.
Indonesian Journal of Medicine (2023), 08(01): 100-113
https://doi.org/10.26911/theijmed.2023.08.01.10
References
Abid JP, Wark AW, Brevet PF, Girault HH (2002). Preparation of silver nanoparticles in solution from a silver salt by laser irradiation. Chem Commun (Camb). 7: 792–793. Doi: 10.1039/b200272h.
Alexander JW (2009). History of the medical use of silver. Surg. Infect. 10(3): 289–292. Doi: 10.1089/sur.2008.9941.
Andrade PF, deFaria AF, daSilva DS, Bonacin JA, Gonçalves M, do C (2014). Structural and morphological investigations of βcyclodextrincoated silver nanoparticles. Colloids and surfaces. 118: 289–297. Doi: 10.1016/j.colsurfb.2014.03.032.
Andriana Y, Xuan TD, Quy TN, Minh TN, Van, TM, Viet TD (2019). Antihyperuricemia, Antioxidant, and Antibacterial Activities of Tridax procumbens L. Foods (Basel, Switzerland), 8(1). Doi: 10.3390/foods8010021.
Atiyeh BS, Costagliola M, Haye SN, Dibo SA (2007). Effect of silver on burn wound infection control and healing: review of the literature. J. Inter. Society Burn Injuries. 33(2): 139–148. Doi: 10.1016/j.burns.2006.06.010.
AyalaNúñez NV, Lara Villegas HH, del Carmen ITL, Rodríguez Padilla C (2009). Silver Nanoparticles Toxicity and Bactericidal Effect Against MethicillinResistant Staphylococcus aureus: Nanoscale Does Matter. J. Nanobiotechnology. 5(1): 2–9. Doi 10.1007/s1203000990291.
Barrow C, Shahidi F (2007). Marine Nutraceuticals and Functional Foods. CRC Press, CAB International. Doi: Doi: 10.1201/9781420015812.
Birla SS, Tiwari VV, Gade AK, Ingle AP, Yadav AP, Rai MK (2009). Fabrication of silver nanoparticles by Phoma glomerate and its combined effect against Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus. Lett. Appl. Microbiol. 48(2): 173–179. Doi: 10.1111/j.1472765X.2008.02510.x.
Braga TM, Rocha L, Chung TY, Oliveira RF, Pinho C, Oliveira AI, Morgado, J., et al. (2021). Azadirachta indica A. Juss. In Vivo ToxicityAn Updated Review. Molecules. 26(2). Doi: 10.3390/molecules26020252.
Brandt O, Mildner M, Egger AE, Groessl M, Rix U, Posch M, Keppler BK, Strupp C., et al. (2012). Nanoscalic silver possesses broadspectrum antimicrobial activities and exhibits fewer toxicological side effects than silver sulfadiazine. Nanomedicine. 8(4): 478–488. Doi: 10.1016/j.nano.2011.07.005
Chinnasamy G, Chandrasekharan S, Bhatnagar S (2019). Biosynthesis of silver nanoparticles from Melia azedarach: Enhancement of antibacterial, wound healing, antidiabetic and antioxidant activities. I. Int. Nanomedicine. 14: 98239836. Doi:10.2147/IJN.S231340.
Chinnasamy G, Chandrasekharan S, Koh TW, Bhatnagar S (2021). Synthesis, Characterization, Antibacterial and Wound Healing Efficacy of Silver Nanoparticles From Azadirachta indica. Front. Microbiol. 12: 1–14. Doi: 10.3389/fmicb.2021.611560.
Covarelli L, Stifano S, Beccari G, Raggi L, Lattanzio VMT, Albertini E (2012). Characterization of Fusarium verticillioides strains isolated from maize in Italy: fumonisin production, pathogenicity, and genetic variability. Food Microbiol. 31(1): 17–24. Doi: 10.1016/j.fm.2012.02.002.
Dorador C, Vila I, Imhoff JF, Witzel KP (2008). Cyanobacterial diversity in Salar de Huasco, a high altitude Saline wetland in northern Chile: an example of geographical dispersion? FEMS Microb. Ecol. 64(3): 419–432. Doi: https://doi.org/10.1111/j.15746941.2008.00483.x.
ElDeeb NM, AboEleneen MA, AlMadboly LA, Sharaf MM, Othman SS, Ibrahim OM, Mubarak MS (2020). Biogenically Synthesized PolysaccharidesCapped Silver Nanoparticles: Immunomodulatory and Antibacterial Potentialities Against Resistant Pseudomonas aeruginosa. Front. Bioeng. Biotechnol. 8: 1–18. Doi: 10.3389/fbioe.2020.00643
Fatima F, Aldawsari MF, Ahmed MM, Anwer MK, Naz M, Ansari MJ, Hamad AM., et al. (2021). Green Synthesized Silver Nanoparticles Using Tridax Procumbens for Topical Application: Excision Wound Model and Histopathological Studies. Pharmaceutic, 13(11). Doi: 10.3390/pharmaceutics13111754.
Gong P, Li H, He X, Wang K, Hu J, Tan W, Zhang S., et al. (2007). Preparation and antibacterial activity of Fe3O4@Ag. Nanotechnology. 18(28), 285604. Doi: 10.1088/09574484/18/28/285604.
Guo S, Dipietro LA (2010). Factors affecting wound healing. J. Dent. Res. 89(3): 219–229. Doi: 10.1177/0022034509359125
Gurunathan S, Han JW, Kwon DN, Kim JH (2014). Enhanced antibacterial and antibiofilm activities of silver nanoparticles against Gram-negative and Gram-positive bacteria. Nanoscale Res. Lett. 9(1): 373. Doi: 10.1186/1556276X9373
Hooijmans CR, Rovers MM, de Vries RB M, Leenaars M, RitskesHoitinga, M, Langendam MW (2014). SYRCLE’s risk of bias tool for animal studies. BMC Med. Res. Methodol. 14: 43. Doi: 10.1186/147122881443.
Jadhav K, Dhamecha D, Bhattacharya D, Patil M (2016). Green and eco-friendly synthesis of silver nanoparticles: Characterization, biocompatibility studies and gel formulation for the treatment of infections in burns. J. Photochem. Photobiol. 155: 109–115. Doi: 10.1016/j.jphotobiol.2016.01.002.
Jaiswal S, Duffy B, Jaiswal AK, Stobie N, McHale P (2010). Enhancement of the antibacterial properties of silver nanoparticles using beta-cyclodextrin as a capping agent. Int. J. Antimicrob. Agents, 36(3), 280–283. Doi: 10.1016/j.ijantimicag.2010.05.006.
Jayakumar R, Prabaharan M, Sudheesh Kumar PT, Nair SV, Tamura H (2011). Biomaterials based on chitin and chitosan in wound dressing applications. Biotechnol. Adv. 29(3): 322–337. Doi: 10.1016/j.biotechadv.2011.01.005.
Judith R, Nithya M, Rose C, Mandal AB. (2010). Application of a PDGFcontaining novel gel for cutaneous wound healing. Life Sci. 87: 1–8. Doi: 10.1016/j.lfs.2010.05.003.
Kalishwaralal K, Banumathi E, Ram Kumar Pandian S, Deepak V, Muniyandi J, Eom SH, Gurunathan S (2009). Silver nanoparticles inhibit VEGF-induced cell proliferation and migration in bovine retinal endothelial cells. Colloids Surf B Biointerfaces 73(1): 51–57. Doi: 10.1016/j.colsurfb.2009.04.025.
Kalishwaralal K, Deepak V, Ramkumarpandian S, Nellaiah H, Sangiliyandi G (2008). Extracellular biosynthesis of silver nanoparticles by the culture supernatant of Bacillus licheniformis. Mater. Lett. 62(29): 4411–4413. Doi: 10.1016/j.matlet.2008.06.051
Khatami M, Pourseyedi S, Khatami M, Hamidi H, Zaeifi M, Soltani L. (2015). Synthesis of silver nanoparticles using seed exudates of Sinapis arvensis as a novel bioresource, and evaluation of their antifungal activity. Bioresour. Bioprocess. 2(1): 19. Doi: 10.1186/s406430150043y
Khorasani MT, Joorabloo A, Moghaddam, A, Shamsi H, MansooriMoghadam, Z (2018). Incorporation of ZnO nanoparticles into heparinized polyvinyl alcohol/chitosan hydrogels for wound dressing application. Int. J. Biol.Macromol. 114: 1203–1215. Doi: 10.1016/j.ijbiomac.2018.04.010.
Kim K.J, Sung WS, Suh BK, Moon SK, Choi JS, Kim JG, Lee DG (2009). Antifungal activity and mode of action of silver nanoparticles on Candida albicans. Biometals : J. Biohem. Med. Metab. Biol. 22(2), 235–242. Doi: 10.1007/s1053400891592.
Kurahashi T, Fujii J (2015). Roles of antioxidative enzymes in wound healing. J. Dev. Biol. 3(2): 57–70. Doi: 10.3390/jdb3020057.
Kvítek L, Panáček A, Soukupová J, Kolář M, Večeřová R, Prucek R, Holecová M., et al. (2008). Effect of Surfactants and Polymers on Stability and Antibacterial Activity of Silver Nanoparticles (NPs). J. Phys. Chem. C. 112(15): 5825–5834. Doi: 10.1021/jp711616v
Lakkim V, Reddy MC, Pallavali RR, Reddy KR, Reddy CV, Inamuddin Bilgrami AL, Lomada D (2020). Green synthesis of silver nanoparticles and evaluation of their antibacterial activity against multidrug-resistant bacteria and wound healing efficacy using a murine model. Antib. 9(12): 1–22. Doi: 10.3390/antibiotics9120902.
Lara HH, AyalaNuñez NV, IxtepanTurrent L, RodriguezPadilla C (2010). Mode of antiviral action of silver nanoparticles against HIV1. J. Nanobiotechnology. 8(1). Doi: 10.1186/1477315581.
Li WR, Xie XB, Shi QS, Duan SS, Ouyang YS, Chen YB (2011). Antibacterial effect of silver nanoparticles on Staphylococcus aureus. J. Biochem. 24(1): 135–141. Doi: 10.1007/s1053401093816.
MacKay D, Miller AL (2003). Nutritional support for wound healing. Alternative Medicine Review : Clin. Ther. 8(4): 359–377.
Mekkawy AI, ElMokhtar MA, Nafady NA, Yousef N, Hamad M, ElShanawany SM, Ibrahim EH., et al. (2017). In vitro and in vivo evaluation of biologically synthesized silver nanoparticles for topical applications: Effect of surface coating and loading into hydrogels. International Nanomed. J. 12: 759–777. Doi: 10.2147/IJN.S124294.
Nadworny PL, Wang J, Tredget EE, Burrell RE (2010). Antiinflammatory activity of nanocrystalline silver-derived solutions in porcine contact dermatitis. J. Inflamm. 7(13.) Doi: 10.1186/14769255713.
Nayak BS, Pinto Pereira LM (2006). Catharanthus roseus flower extract has wound-healing activity in Sprague Dawley rats. BMC Complementary and Altern. Med. Stud. 6(41). Doi: 10.1186/14726882641.
Oei JD, Zhao WW, Chu L, DeSilva MN, Ghimire A, Rawls HR, Whang K (2012). Antimicrobial acrylic materials with in situ generated silver nanoparticles. J. Biomed. Mater. Res . Part B, Applied Biomaterials. 100(2): 409–415. Doi: 10.1002/jbm.b.31963.
Pal G, Rai P, Pandey A (2019). Chapter 1 Green synthesis of nanoparticles: A greener approach for a cleaner future. In A. K. Shukla & S. B. T.G. S. Iravani Characterization and Applications of Nanoparticles (Eds.). Micro Nano Lett. 1–26. Doi: 10.1016/B9780081025796.000010.
Park Y (2014). New paradigm shift for the green synthesis of antibacterial silver nanoparticles utilizing plant extracts. Toxicol. Res. 30(3): 169–178. Doi: 10.5487/TR.2014.30.3.169.
Parwani L (2021). Potential of Cyanobacteria in Wound Healing (M. Shrivastava (ed.); p. Ch. 3). J Ilm. intech. Doi: 10.5772/intechopen.98521.
Percival SL, Bowler PG, Dolman J (2007). Antimicrobial activity of silver-containing dressings on wound microorganisms using an in vitro biofilm model. Int. Wound J. 4(2): 186–191. Doi: 10.1111/j.1742481X.2007.00296.x.
PérezDíaz M, AlvaradoGomez E, MagañaAquino M, SánchezSánchez R, Velasquillo C, Gonzalez, C, GanemRondero A., et al. (2016). Antibiofilm activity of chitosan gels formulated with silver nanoparticles and their cytotoxic effect on human fibroblasts. Materials Science and Engineering. C, Materials for Biological Applications. 60: 317–323. Doi: 10.1016/j.msec.2015.11.036.
Priya VV, Periadurai N, Karunakaran T, Hussain S, Krishna Mohan S, Jiao X (2021). Green synthesis of silver nanoparticles from aqueous extract of Scutellaria barbata and coating on the cotton fabric for antimicrobial applications and wound healing activity in fibroblast cells (L929). Saudi J. Biol. Sci. Doi: 10.1016/j.sjbs.2021.05.007.
Pryshchepa O, Pomastowski P, Buszewski B (2020). Silver nanoparticles: Synthesis, investigation techniques, and properties. Adv. Colloid. Doi: 10.1016/j.cis.2020.102246
Qian Y, Xu C, Xiong W, Jiang N, Zheng Y, He X, Ding F., et al. (2021). Dual crosslinked organic-inorganic hybrid hydrogels J. Chem. Eng.
Rahisuddin, AlThabaiti SA, Khan Z, Manzoor N (2015). Biosynthesis of silver nanoparticles and its antibacterial and antifungal activities towards Gram-positive, Gram-negative bacterial strains and different species of Candida fungus. Bioprocess Biosyst. Eng. 38(9), 1773–1781. Doi: 10.1007/s0044901514183.
Rai M, Yadav A, Gade A (2009). Silver nanoparticles as a new generation of antimicrobials. Biotechnol. Adv. 27(1): 76–83. Doi: 10.1016/j.biotechadv.2008.09.002.
She J, Yan H, Yang J, Xu W, Su Z (2019). croFGD: Catharanthus roseus Functional Genomics Database. Front. Genet. 10: 238. Doi: 10.3389/fgene.2019.00238.
Shrivastava S, Bera T, Singh SK, Singh G, Ramachandra Rao P, Dash D (2009). Characterization of antiplatelet properties of silver nanoparticles. ACS Nano. 3(6): 1357–1364. Doi: 10.1021/nn900277t.
Singh R, Parihar P, Singh M, Bajguz A, Kumar J, Singh S, Singh VP., et al. (2017). Uncovering Potential Applications of Cyanobacteria and Algal Metabolites in Biology, Agriculture and Medicine: Current Status and Future Prospects. Front. Microbiol. 8: 515. Doi: 10.3389/fmicb.2017.00515.
Taton A, Grubisic S, Balthasart P, Hodgson DA, LaybournParry J, Wilmotte A (2006). Biogeographical distribution and ecological ranges of benthic cyanobacteria in East Antarctic lakes. Microbiol Lett. 57(2): 272–289. Doi: 10.1111/j.15746941.2006.00110.x.
Thakur R, Jain N, Pathak R, Sandhu SS (2011). Practices in wound healing studies of plants. Evidence-Based Complementary and Alternative Medicine : eCAM. Doi: 10.1155/2011/438056.
Thi PL, Lee Y, Tran DL, Thi TTH, Kang JIl, Park KM, Park KD (2020). In situ forming and reactive oxygen species scavenging gelatin hydrogels for enhancing wound healing efficacy. Acta Biomater. 103: 142–152. Doi: 10.1016/j.actbio.2019.12.009
Thorley AJ, Tetley TD (2013). New perspectives in nanomedicine. Pharmacol. 140(2): 176–185. Doi: 10.1016/j.pharmthera.2013.06.008.
Velnar T, Bailey T, Smrkolj V (2009). The wound healing process: an overview of the cellular and molecular mechanisms. Int. J. Med. Res. 37(5): 1528–1542. Doi: 10.1177/147323000903700531.
Wang L, Yang K, Li X, Zhang X, Zhang D, Wang LN, Lee CS (2021). A double crosslinked self-healing antibacterial hydrogel with enhanced mechanical performance for wound treatment. Acta Biomater. 124: 139–152. Doi: 10.1016/j.actbio.2021.01.038.
Wen L, Zeng P, Zhang L, Huang W, Wang H, Chen G (2016). Symbiosis theory directed green synthesis of silver nanoparticles and their application in infected wound healing. Int. J. Nanomedicine. Doi: 10.2147/IJN.S106662.
Widiyanto A, Murti B, Soemanto RB (2018). Multilevel Analysis on The Effect of SocioCultural, Lifestyle factors, and School Environment, on the Risk of Overweight in Adolescents, Karanganyar District, Central Java. J. Epidemiol. Public Health. 3(1): 94104. Doi: 10.26911/jepublichealth.2018.03.01.08.
Wollina U, Voicu C, Gianfaldoni S, Lotti, T, França K, Tchernev G (2018). Arthrospira PlatensisPotential in Dermatology and Beyond. Open Access Macedonian J. Med. Sci. 6(1): 176–180. Doi: 10.3889/oamjms.2018.033.
Younis NS, El Semary NA, Mohamed ME (2021). Silver nanoparticles green synthesis via cyanobacterium Phormidium sp.: Characterization, wound healing, antioxidant, antibacterial, and anti-inflammatory activities. Eur Rev Med. 25(7): 3083. Doi: 10.26355/eurrev_202104_25563.
Younis NS, Mohamed ME, El Semary NA (2022). Green Synthesis of Silver Nanoparticles by the Cyanobacteria Synechocystis sp.: Characterization, Antimicrobial, and Diabetic WoundHealing Actions. Mar. Drugs 20(1). Doi: 10.3390/md20010056.
Zandi N, Dolatyar B, Lotfi R, Shallageh Y, Shokrgozar MA, Tamjid E, Annabi N., et al. (2021). Biomimetic nanoengineered scaffold for enhanced full-thickness cutaneous wound healing. Acta Biomater., 124, 191–204. Doi: 10.1016/j.actbio.2021.01.029.
